Preconception and Prenatal Environmental Factors Associated with Communication Impairments in 9 Year Old Children Using an Exposome-Wide Approach

Preconception and Prenatal Environmental Factors Associated with Communication Impairments in 9 Year Old Children Using an Exposome-Wide Approach
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  RESEARCHARTICLE Preconception and Prenatal EnvironmentalFactors Associated with CommunicationImpairments in 9 Year Old Children Using anExposome-Wide Approach ColinD. Steer 1 * , Patrick Bolton 2 , Jean Golding 3 1  MRCintegrativeepidemiologicalunit,SchoolofSocialandCommunityMedicine,UniversityofBristol,Bristol,UnitedKingdom, 2  King ’ s CollegeLondon,InstituteofPsychiatry,London,UnitedKingdom, 3  CentreforChildandAdolescentHealth,SchoolofSocialandCommunityMedicine,UniversityofBristol,Bristol,UnitedKingdom * Abstract Although speech and languagedeficits are common inchildrenand stronglyassociatedwith pooreducational and social outcomes,little attentionhas beenpaidto theantecedents.In thisstudy we used theinformation from the Avon Longitudinal Study of Parentsand Chil-dren to examine preconception and prenatal environmentalrisk factors that were related tocommunicationdifficulties in children using the Children ’ s Communication Checklist (CCC).We usedan exposome-wideapproachto identifyenvironmental factors univariably associ-ated with the CCC. Takingaccount of theFalse Discovery rate, we useda Pvalueof0.000157to identify 621 of 3855items tested. These were then subjectedto a series ofstepwise linear regressionanalyses, firstlywithin10domains: personalcharacteristics,health, development, education,socio-economicvariables, lifestyle, homeand social envi-ronments, life events and chemical and other exposures; and then with the predictivevari-ables from eachdomain. The final model consisted of 19variables independentlyassociatedwith the communicationscale. These variables suggested 6possible mecha-nisms: stressorsprimarily associated with socio-economicdisadvantage although otherlife-style choices such asa social network of family or friends can ameliorate these effects;indicators of futureparentingskills primarily associatedwith aspects of parental personality;aspects of thehomeenvironment; poor maternalhealth with anovelfinding concerning ma-ternal hearing loss; andmaternal education which was partially mediated bythe child ’ s IQ.Finally, there may bea mechanism via the maternal diet inpregnancyinparticular thecon-sumption of fattyor processed foods. Thisis thesubjectof ongoing investigation. PLOSONE|DOI:10.1371/journal.pone.0118701 March4,2015 1/26 a11111 OPENACCESS Citation:  Steer CD, Bolton P, Golding J (2015)Preconception and Prenatal Environmental FactorsAssociated with Communication Impairments in9 Year Old Children Using an Exposome-WideApproach. PLoS ONE 10(3): e0118701. doi:10.1371/  journal.pone.0118701 Academic Editor:  Hanjun Liu, Sun Yat-senUniversity, CHINA  Received:  July 28, 2011 Accepted:  January 23, 2015 Published:  March 4, 2015 Copyright:  © 2015 Steer et al. This is an openaccess article distributed under the terms of theCreative Commons Attribution License, which permitsunrestricted use, distribution, and reproduction in anymedium, provided the srcinal author and source arecredited. Funding:  The UK Medical Research Council (MRC),the Wellcome Trust and the University of Bristolcurrently provide core support for ALSPAC. Thisstudy was funded by the UK MRC —  grant G0800523.Patrick Bolton was supported by The NIHRBiomedical Research Centre in Mental Health at theSouth London & Maudsley Hospital. Version 3.01 of the exposome was partially funded by the WaterlooFoundation. The funders had no role in study design,data collection and analysis, decision to publish, or preparation of the manuscript.  Introduction Communication impairments relate not only to the fluency and intelligibility of speech butalso to expressive and receptive language impairments. Language impairments can includethose involving semantics, such as subtle nuances, as well as pragmatic aspects of language in asocial context [1]. Twin studies have suggested that, although children must be exposed to lan- guage in their environment in order to learn it, communication impairments have a major he-redity component [2,3]. However, the low estimates of environmental influences may be misleading for two reasons. First, these studies may underestimate the importance of environ-mental effects due to gene-environment interactions being subsumed into the heritability term[4]. Second, different impairments may have varying genetic components. Hence, while speechimpairments may have high heritability, language impairments may be largely environmentally determined [5]. A few studies have assessed prenatal exposures that may have an effect on the developmentof effective communication in the child. Positive associations have been demonstrated for ma-ternal smoking in pregnancy with lower language scores in longitudinal studies of childrenaged 3 – 12 years [6 – 8], as well as in a case-control study of children with specific language im-pairment [9]. Among studies of illicit drugs, there have been reports of associations between lower general language scores and maternal use of cocaine in pregnancy [10,11]. A study of an- ticonvulsants used prenatally among women with epilepsy demonstrated an association be-tween phenytoin and both the verbal comprehension and expressive language scores on theReynell scales, which was not found with a different anticonvulsant [12]. Another study found an association between sodium valproate exposure in the 1 st trimester with language im-pairment [13]. A comparison of 5 – 6 year olds whose mothers had had prenatal iodine supple-mentation in an iodine-deficient area in China showed that delay in expressive language wasreduced compared with non-supplemented controls [14]. Biomarkers have also shown evi-dence of possible prenatal mechanisms — for example examination of cord blood of girls in theRaine study showed an association between testosterone levels and subsequent pragmatic lan-guage score of the child [15]. However, most of these studies were either based on relatively small numbers or failed to take account of socio-economic and other factors that may haveinfluenced the associations; additionally they did not distinguish specific language difficultiesfrom those associated with more general developmental delay.In the present study we take advantage of the prospective data collected in the Avon Longi-tudinal Study of Parents and Children (ALSPAC) which included questions from the Chil-dren ’ s Communication Checklist (CCC), specifically designed to quantify communicationdifficulties that affect everyday life and which may not be detectable by standardised tests [1]. Here we begin by considering factors prior to the birth of the study child reflecting aspects of the grandparents and parental histories starting from their respective births. These data havethe advantage that parental responses are collected before the parents can detect any problemin their child, and hence are not influenced in their responses by any stress their child ’ s condi-tion may initiate. Other more objective data from biosamples during pregnancy arealso analysed.Since the preconception and prenatal environmental factors that may influence communi-cation impairments are largely uncharted, we use an exposome-wide approach [16]. This is similar to the approach taken in genome wide association studies (GWAS), being hypothesisfree. Rather than testing already formulated hypotheses, this approach examines associationsto generate hypotheses for replication in other studies. Although largely considered for assaysof biological markers [16,17], it has recently been expanded to include lifestyle (such as diet, smoking and exercise) and the dynamic interaction with our surroundings [18,19]. Here we Environmental Factors&CommunicationImpairmentsPLOSONE|DOI:10.1371/journal.pone.0118701 March4,2015 2/26 Competing Interests:  The authors have declaredthat no competing interests exist.  expand the concept further to look additionally at questionnaire based information on the en- vironment in its broadest sense including aspects of parental and grandparental psychosocialtraits and health. Methods ALSPACsample The prospective longitudinal cohort study, ALSPAC, was designed with the specific aim of identifying environmental and genetic factors, and the interaction between them, that influencethe health and development of the child. Information was collected from around 14000 preg-nant women, resident in the county of Avon, with expected date of delivery between 1 st April1991 and 31 st December 1992 [20]. Ethicsstatement Ethical approval for the study was obtained from the ALSPAC Ethics and Law Committee andthe Southmead, Frenchay, UBHT and Weston Research Ethics Committees. Written consentwas obtained from participants to allow use of anonymised linked biological data for researchby bona fide scientists. Children ’ sCommunication Checklist At age 9 the study mother completed a questionnaire which included 7 of the 9 scales of thefirst version of the Children ’ s Communication Checklist (CCC) [1]. This checklist was de- signed to assess aspects of communication that are not readily assessed by conventional stan-dardised tests including aspects of speech and syntax, as well as pragmatic aspects such asover-literal interpretation of stereotyped language. Although the CCC was initially designed toidentify pragmatic difficulties, it has been shown to be good at discriminating a wide range of language and communication problems from typical development [21]. Questions were not ad- ministered on the subscales  Social relationships  and  Interests . The present analysis uses a totalCCC score obtained by summing the 7 communication scales, with higher scores indicating more typical behaviour. The score had a skewed distribution (Fig. 1). Although the total scorehad a feasible range of 126 – 232, no children were observed with the most extreme scores (ob-served range 144 – 230). ALSPACexposome Version 3.01 of the exposome scan includes 3965 variables relating to the preconception andprenatal period as well as details of the study parents and their family background collectedfrom questionnaires completed by the parents (see S1 Methods). Some 110 variables such as il-licit drug use, schizophrenia amongst study parents and grandparents and parental birth de-fects, had only the absence of these features reported within the sample defined by the CCCoutcome and have been excluded from subsequent analyses. The main variables discussed inthis study are described below classified according to 10 domains. (i)Personalcharacteristicsof parents This domain included variables related to personal characteristics such as personality, attitudesand beliefs. Babies need stimulation to develop — assessed on a 4-point scale ranging from  disagree  to agree  as reported by the mother. Environmental Factors&CommunicationImpairmentsPLOSONE|DOI:10.1371/journal.pone.0118701 March4,2015 3/26  Separation anxiety   and  Total sensitivity  — five subscales and a total score derived from the36 questions on personality using the Interpersonal Sensitivity Measure (IPSM) [22]. High scores indicate greater sensitivity. These two derived scores related to the mother. Locus of control score — a score based upon 12 questions devised to assess whether the indi- vidual believes that events resulted primarily from his/her own behaviour (internalised locus)or whether they arose due to chance or fate (externalised locus) [23]. High scores indicate ex- ternalising locus. Both maternal and partner reported scores were selected. Bottle feeding more convenient  — one of 5 questions concerning attitudes to breastfeeding with a range of responses from  strongly disagree  to  strongly agree . This question was selected inpreference to the combined score. (ii)Health ofparents Night coughing  — absence of, occasional or frequent coughing at night by the mother over thelast 2 years.  Any hearing loss — derived from any reported problems ( occasional problems (eg infectionsor glue ear)  to  I cannot hear much at all  ) in either ear for the mother.  Maternal Depression — measured depressive symptoms using either the 10 items of the Edin-burgh Postnatal Depression Scale (EPDS) [24] or the 8 items from the Crown-Crisp (CCEI) Fig1. DistributionoftheTotalCCCScore(N =7942). doi:10.1371/journal.pone.0118701.g001 Environmental Factors&CommunicationImpairmentsPLOSONE|DOI:10.1371/journal.pone.0118701 March4,2015 4/26  scale [25]. At 18w gestation, both derived scores were selected but in addition two individualitems from the CCEI were also included. At 32w gestation, only one item from the EPDS ( un-necessary self blame ) was selected. Somatic symptoms — two items from the CCEI at 18w and one item at 32w were selected asreported by the mother. Feel good score — 7 questions on subjective health, for instance how irritable or nervous,were combined to create this score. Separate scores relating to the mother as reported by herself and her partner were included. One question relating to the partner (looking attractive as re-ported by the mother) was also selected. An additional variable also assessed how these 7 traitschanged since the mother became pregnant as reported by the partner. (iii) Development This domain is mostly populated by variables relating to the child ’ s development. Howeverthere were a few questions assessing the parents ’  own childhood development.  Mother received child guidance  was selected. (iv)Education Variables related to the achievement of national qualifications at 16y and 18y for the motherand a university degree for the partner were selected.  Mother has no qualification  and  Partner has unknown qualification  were also included. All information was reported by the mother. Acomposite variable of the mother ’ s highest qualification was also selected but is typically usedas an indicator of socio-economic status (see (v) below). (v) Socio-economic  Maternal social class — ranging from class I (professional /executive) to class V (unskilled) [26]  Maternal education — was the highest educational level obtained by late pregnancy. Thequalifications obtained were scored on a 5-point scale from the lowest (none or CSE) to highest(University degree). Financial difficulties — a scale derived from maternal reports on the difficulty the family hadin affording items such as food, housing, heating, clothes and items for the baby. Lowest level of accommodation — ranged from basement to 16 th floor. Frequency of car use — usage by the mother on a 3-point scale ranging from  never   to  everyday  . (vi)Lifestyle There were 11 variables selected. These related to the mother mainly in the 3 rd trimester. Of these 7 related to diet. Cola intake — number of cans of cola drunk in 1 st trimester by mother Drinking of milk ,  total  — the number of glasses drunk on weekdays and weekends at18 weeks gestation. Use of sterilised milk — with responses  never  ,  sometimes  and  usually  . Eating offal  — the eating of liver, heart, kidney or liver pate with five responses ranging from never or rarely   to  more than once per day  . Health conscious dietary factor   and  Processed dietary factor  — Maternal dietary patterns werederived from the Food Frequency Questionnaire at 32 weeks gestation using principal compo-nent analysis [27]. Of the 5 dietary factors identified from this analysis, two were significant — health conscious diet   comprising a diet with higher consumption of salad, fruit, rice, pasta,breakfast cereals, fish, eggs, pulses, fruit juices, white meat and non-white bread; and a Environmental Factors&CommunicationImpairmentsPLOSONE|DOI:10.1371/journal.pone.0118701 March4,2015 5/26
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